He made his England debut against Argentina in 1997 and later his first match at Twickenham was as a half-time replacement for the Bath hooker Andy Long in Clive Woodward's first match in charge against the Wallabies; Long was young and clearly out of his depth. Cockerill's performance earned him a starting place against New Zealand, where he stood up to Norm Hewitt during the haka (see book cover).

A dip in form led him to lose his first choice hooking position at Leicester to Dorian West. He was also dropped from the England side after criticising Woodward in his book entitled In Your Face. He subsequently moved to France, but signed again for Leicester for the 2004–5 season.

In 2005 he was appointed forwards coach at Leicester Tigers succeeding John Wells.[3]